A dense linkage map for a large repetitive genome: discovery of the sex-determining region in hybridizing fire-bellied toads (Bombina bombina and Bombina variegata)
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem
Grantová podpora
T32 HG000047
NHGRI NIH HHS - United States
R01 GM086321
NIGMS NIH HHS - United States
R01 HD080708
NICHD NIH HHS - United States
T32 GM007127
NIGMS NIH HHS - United States
PubMed
34849761
PubMed Central
PMC8664441
DOI
10.1093/g3journal/jkab286
PII: 6353606
Knihovny.cz E-zdroje
- Klíčová slova
- anurans, genome assembly, hybrid zone, large-scale synteny, linkage map, population pileups diplotyping, segregation distortion, sex-determining region, targeted capture,
- MeSH
- genetická vazba MeSH
- genom * MeSH
- larva MeSH
- mapování chromozomů MeSH
- žáby * genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
Genomic analysis of hybrid zones offers unique insights into emerging reproductive isolation and the dynamics of introgression. Because hybrid genomes consist of blocks inherited from one or the other parental taxon, linkage information is essential. In most cases, the spectrum of local ancestry tracts can be efficiently uncovered from dense linkage maps. Here, we report the development of such a map for the hybridizing toads, Bombina bombina and Bombina variegata (Anura: Bombinatoridae). Faced with the challenge of a large (7-10 Gb), repetitive genome, we set out to identify a large number of Mendelian markers in the nonrepetitive portion of the genome that report B. bombina vs B. variegata ancestry with appropriately quantified statistical support. Bait sequences for targeted enrichment were selected from a draft genome assembly, after filtering highly repetitive sequences. We developed a novel approach to infer the most likely diplotype per sample and locus from the raw read mapping data, which is robust to over-merging and obviates arbitrary filtering thresholds. Validation of the resulting map with 4755 markers underscored the large-scale synteny between Bombina and Xenopus tropicalis. By assessing the sex of late-stage F2 tadpoles from histological sections, we identified the sex-determining region in the Bombina genome to 7 cM on LG5, which is homologous to X. tropicalis chromosome 5, and inferred male heterogamety. Interestingly, chromosome 5 has been repeatedly recruited as a sex chromosome in anurans with XY sex determination.
Department of Comparative Anatomy Jagiellonian University 30 387 Kraków Poland
Department of Molecular and Cell Biology University of California Berkeley Berkeley 94720 CA USA
Tree of Life Programme Wellcome Sanger Institute Hinxton Cambridge CB10 1SA UK
Zobrazit více v PubMed
Baird SJE. 1995. A simulation study of multilocus clines. Evolution. 49:1038–1045. PubMed
Baird SJE. 2006. Fisher’s markers of admixture. Heredity (Edinb). 97:81–83. 10.1038/sj.hdy.6800850. PubMed DOI
Baker RJ, Bickham JW.. 1980. Karyotypic evolution in bats: evidence of extensive and conservative chromosomal evolution in closely related taxa. Syst Biol. 29:239–253. 10.1093/sysbio/29.3.239. DOI
Bao W, Kojima KK, Kohany O.. 2015. Repbase update, a database of repetitive elements in eukaryotic genomes. Mob DNA. 6:11. 10.1186/s13100-015-0041-9. PubMed DOI PMC
Barton NH. 1979. Gene flow past a cline. Heredity. 43:333–339.
Barton NH. 1983. Multilocus clines. Evolution. 37:454–471. PubMed
Benjamini Y, Hochberg Y.. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B. 57:289–300.
Brelsford A, Lavanchy G, Sermier R, Rausch A, Perrin N.. 2016b. Identifying homomorphic sex chromosomes from wild-caught adults with limited genomic resources. Mol Ecol Resour. 17:752–759. 10.1111/1755-0998.12624. PubMed DOI
Brelsford A, Rodrigues N, Perrin N.. 2016a. High-density linkage maps fail to detect any genetic component to sex determination in a Rana temporaria family. J Evol Biol. 29:220–225. 10.1111/jeb.12747. PubMed DOI
Brelsford A, Stöck M, Betto-Colliard C, Dubey S, Dufresnes C, et al.2013. Homologous sex chromosomes in three deeply divergent anuran species. Evolution. 67:2434–2440. PubMed
Broad Institute 2019. Picard Toolkit. http://broadinstitute.github.io/picard/
Bush GL, Case SM, Wilson AC, Patton JL.. 1977. Rapid speciation and chromosomal evolution in mammals. Proc Natl Acad Sci USA. 74:3942–3946. doi:10.1073/pnas.74.9.3942. PubMed DOI PMC
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, et al.2009. BLAST+: architecture and applications. BMC Bioinformatics. 10:421. 10.1186/1471-2105-10-421. PubMed DOI PMC
Carneiro M, Baird SJE, Afonso S, Ramirez E, Tarroso P, et al.2013. Steep clines within a highly permeable genome across a hybrid zone between two subspecies of the European rabbit. Mol Ecol. 22:2511–2525. 10.1111/mec.12272. PubMed DOI PMC
Charlesworth B, Charlesworth D.. 2000. The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci. 355:1563–1572. 10.1098/rstb.2000.0717. PubMed DOI PMC
Charlesworth D, Charlesworth B, Marais G.. 2005. Steps in the evolution of heteromorphic sex chromosomes. Heredity (Edinb). 95:118–128. 10.1038/sj.hdy.6800697. PubMed DOI
Charlesworth D. 2019. Young sex chromosomes in plants and animals. New Phytol. 224:1095–1107. 10.1111/nph.16002. PubMed DOI
Chevalier FD, Valentim CL, LoVerde PT, Anderson TJ.. 2014. Efficient linkage mapping using exome capture and extreme QTL in schistosome parasites. BMC Genomics. 15:617. 10.1186/1471-2164-15-617. PubMed DOI PMC
Chu C, Nielsen R, Wu Y.. 2016. REPdenovo: inferring de novo repeat motifs from short sequence reads. PLoS One. 11:e0150719. 10.1371/journal.pone.0150719. PubMed DOI PMC
Corbett-Detig R, Nielsen R.. 2017. A hidden Markov model approach for simultaneously estimating local ancestry and admixture time using next generation sequence data in samples of arbitrary ploidy. PLoS Genet. 13:e1006529. 10.1371/journal.pgen.1006529. PubMed DOI PMC
Coyne JA, Orr HA.. 2004. Speciation. Sunderland, MA: Sinauer Associates.
Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, et al.2011. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet. 12:499–510. PubMed
Dufresnes C, Litvinchuk SN, Rozenblut‐Kościsty B, Rodrigues N, Perrin N, et al.2020. Hybridization and introgression between toads with different sex chromosome systems. Evol Lett. 4:444–456. 10.1002/evl3.191. PubMed DOI PMC
Dufresnes C, Majtyka T, Baird SJE, Gerchen JF, Borzée A, et al.2016. Empirical evidence for large X-effects in animals with undifferentiated sex chromosomes. Sci Rep. 6:21029. 10.1038/srep21029. PubMed DOI PMC
Edwards RJ, Tuipulotu DE, Amos TG, O'Meally D, Richardson MF, et al.2018. Draft genome assembly of the invasive cane toad, Rhinella marina. Gigascience. 7:giy095.. doi:10.1093/gigascience/giy095. PubMed DOI PMC
Eggert C. 2004. Sex determination: the amphibian models. Reprod Nutr Dev. 44:539–549. 10.1051/rnd:2004062. PubMed DOI
Feng Y-J, Blackburn DC, Liang D, Hillis DM, Wake DB, et al.2017. Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous–Paleogene boundary. Proc Natl Acad Sci USA. 114:E5864–E5870. 10.1073/pnas.1704632114. PubMed DOI PMC
Fishman L, McIntosh M.. 2019. Standard deviations: the biological bases of transmission ratio distortion. Annu Rev Genet. 53:347–372. 10.1146/annurev-genet-112618-043905. PubMed DOI
Fontaine A, Filipović I, Fansiri T, Hoffmann AA, Cheng C, et al.2017. Extensive genetic differentiation between homomorphic sex chromosomes in the mosquito vector, Aedes aegypti. Genome Biol Evol. 9:2322–2335. 10.1093/gbe/evx171. PubMed DOI PMC
Furman BLS, Evans BJ.. 2016. Sequential turnovers of sex chromosomes in African clawed frogs (Xenopus) suggest some genomic regions are good at sex determination. G3 (Bethesda). 6:3625–3633. 10.1534/g3.116.033423. PubMed DOI PMC
Furman BLS, Cauret CMS, Knytl M, Song X-Y, Premachandra T, et al.2020. A frog with three sex chromosomes that co-mingle together in nature: Xenopus tropicalis has a degenerate W and a Y that evolved from a Z chromosome. PLoS Genet. 16:e1009121. 10.1371/journal.pgen.1009121. PubMed DOI PMC
Furman BLS, Evans BJ.. 2018. Divergent evolutionary trajectories of two young, homomorphic, and closely related sex chromosome systems. Genome Biol Evol. 10:742–755. 10.1093/gbe/evy045. PubMed DOI PMC
Gammerdinger WJ, , Kocher TD.. 2018. Unusual Diversity of Sex Chromosomes in African Cichlid Fishes. Genes (Basel). 9:10.3390/genes9100480 30287777 PubMed DOI PMC
Glenn TC, Nilsen RA, Kieran TJ, Sanders JG, Bayona-Vásquez NJ, et al.2019. Adapterama I: universal stubs and primers for 384 unique dual-indexed or 147,456 combinatorially-indexed Illumina libraries (iTru & iNext). PeerJ. 7:e7755. 10.7717/peerj.7755. PubMed DOI PMC
Gosner KL. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica. 16:183–190.
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, et al.2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 29:644–652. PubMed PMC
Graves JAM, Peichel CL.. 2010. Are homologies in vertebrate sex determination due to shared ancestry or to limited options? Genome Biol. 11:205. 10.1186/gb-2010-11-4-205. PubMed DOI PMC
Gravel S. 2012. Population genetics models of local ancestry. Genetics. 191:607–619. 10.1534/genetics.112.139808. PubMed DOI PMC
Gregory TR. 2021. Animal Genome Size Database. http://www.genomesize.com.
Guerrero RC, Kirkpatrick M, Perrin N.. 2012. Cryptic recombination in the ever-young sex chromosomes of Hylid frogs. J Evol Biol. 25:1947–1954. PubMed
Haenel Q, Laurentino TG, Roesti M, Berner D.. 2018. Meta-analysis of chromosome-scale crossover rate variation in eukaryotes and its significance to evolutionary genomics. Mol Ecol. 27:2477–2497. 10.1111/mec.14699. PubMed DOI
Harvey MG, Smith BT, Glenn TC, Faircloth BC, Brumfield RT.. 2016. Sequence capture versus restriction site associated DNA sequencing for shallow systematics. Syst Biol. 65:910–924. 10.1093/sysbio/syw036. PubMed DOI
Hedtke SM, Morgan MJ, Cannatella DC, Hillis DM.. 2013. Targeted enrichment: maximizing orthologous gene comparisons across deep evolutionary time. PLoS One. 8:e67908. 10.1371/journal.pone.0067908. PubMed DOI PMC
Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, et al.2010. The genome of the Western clawed frog Xenopus tropicalis. Science. 328:633–636. 10.1126/science.1183670. PubMed DOI PMC
Herpin A, Schartl M.. 2015. Plasticity of gene-regulatory networks controlling sex determination: of masters, slaves, usual suspects, newcomers, and usurpators. EMBO Rep. 16:1260–1274. 10.15252/embr.201540667. PubMed DOI PMC
Hofman S, Szymura JM.. 2000. Inheritance of allozyme loci in Bombina: second linkage group established. Biochem Genet. 38:259–266. PubMed
Hunter SS, Lyon RT, Sarver BAJ, Hardwick K, Forney LJ, et al.2015. Assembly by Reduced Complexity (ARC): a hybrid approach for targeted assembly of homologous sequences. bioRxiv 014662. 10.1101/014662. DOI
Hutter CR, Cobb KA, Portik DM, Travers SL, Wood PL, et al.2019. FrogCap: a modular sequence capture probe set for phylogenomics and population genetics for all frogs, assessed across Multiple Phylogenetic Scales . bioRxiv 825307. 10.1101/825307. PubMed DOI
Hvala JA, Frayer ME, Payseur BA.. 2018. Signatures of hybridization and speciation in genomic patterns of ancestry. Evolution. 72:1540–1552. 10.1111/evo.13509. PubMed DOI PMC
Janzen T, Nolte AW, Traulsen A.. 2018. The breakdown of genomic ancestry blocks in hybrid lineages given a finite number of recombination sites. Evolution. 72:735–750. 10.1111/evo.13436. PubMed DOI PMC
Jeffries DL, Lavanchy G, Sermier R, Sredl MJ, Miura I, et al.2018. A rapid rate of sex-chromosome turnover and non-random transitions in true frogs. Nat Commun. 9:4088. 10.1038/s41467-018-06517-2. PubMed DOI PMC
Jones MR, Good JM.. 2016. Targeted capture in evolutionary and ecological genomics. Mol Ecol. 25:185–202. 10.1111/mec.13304. PubMed DOI PMC
Jones P, Binns D, Chang H-Y, Fraser M, Li W, et al.2014. InterProScan 5: genome-scale protein function classification. Bioinformatics. 30:1236–1240. 10.1093/bioinformatics/btu031. PubMed DOI PMC
Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, et al.2005. Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 110:462–467. 10.1159/000084979. PubMed DOI
Kajitani R, Toshimoto K, Noguchi H, Toyoda A, Ogura Y, et al.2014. Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Res. 24:1384–1395. 10.1101/gr.170720.113. PubMed DOI PMC
Kawamura T, Nishioka M.. 1977. Aspects of the reproductive biology of Japanese anurans. In:Taylor DH, Guttman SI, editors. The Reproductive Biology of Amphibians. New York, NY: Plenum Press. p. 103–139.
Kiernan JA. 1990. Histological and Histochemical Methods. Oxford: Pergamon Press.
Kofler R, Orozco-terWengel P, Maio ND, Pandey RV, Nolte V, et al.2011. PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS One. 6:e15925. 10.1371/journal.pone.0015925. PubMed DOI PMC
Kohany O, Gentles AJ, Hankus L, Jurka J.. 2006. Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics. 7:474. PubMed PMC
Krzywinski MI, Schein JE, Birol I, Connors J, Gascoyne R, et al.2009. Circos: an information aesthetic for comparative genomics. Genome Res. 19:1639–1645. 10.1101/gr.092759.109. PubMed DOI PMC
Langmead B, Salzberg SL.. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods. 9:357–359. 10.1038/nmeth.1923. PubMed DOI PMC
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al.; 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 25:2078–2079. 10.1093/bioinformatics/btp352. PubMed DOI PMC
Li J, Yu H, Wang W, Fu C, Zhang W, et al.2019a. Genomic and transcriptomic insights into molecular basis of sexually dimorphic nuptial spines in Leptobrachium leishanense. Nat Commun. 10:5551. 10.1038/s41467-019-13531-5. PubMed DOI PMC
Li Y, Ren Y, Zhang D, Jiang H, Wang Z, et al.2019b. Chromosome-level assembly of the mustache toad genome using third-generation DNA sequencing and Hi-C analysis. Gigascience. 8:giz114. doi:10.1093/gigascience/giz114. PubMed DOI PMC
Ma W-J, Veltsos P.. 2021. The diversity and evolution of sex chromosomes in frogs. Genes. 12:483. 10.3390/genes12040483. PubMed DOI PMC
Macholán M, Baird SJE, Munclinger P, Dufková P, Bímová B, et al.2008. Genetic conflict outweighs heterogametic incompatibility in the mouse hybrid zone? BMC Evol Biol. 8:271. 10.1186/1471-2148-8-271. PubMed DOI PMC
Manilo VV, Radchenko VI, Reminnyi VJ.. 2006. Materials of karyology of the fire-bellied toad Bombina bombina and B. variegata (Amphibia, Anura, Bombinatoridae) from the territory of Ukraine. Vestnik Zoologii. 40:529–533.
Margarido GRA, Souza AP, Garcia A. A F.. 2007. OneMap: software for genetic mapping in outcrossing species. Hereditas. 144:78–79. 10.1111/j.2007.0018-0661.02000.x. PubMed DOI
Marks J. 1983. Rates of karyotype evolution. Syst Zool. 32:207–209. 10.2307/2413282. DOI
Maroja LS, Larson EL, Bogdanowicz SM, Harrison RG.. 2015. Genes with restricted introgression in a field cricket (Gryllus firmus/Gryllus pennsylvanicus) hybrid zone are concentrated on the X Chromosome and a single autosome. G3 (Bethesda). 5:2219–2227. 10.1534/g3.115.021246. PubMed DOI PMC
McCartney‐Melstad E, Mount GG, Shaffer HB.. 2016. Exon capture optimization in amphibians with large genomes. Mol Ecol Resour. 16:1084–1094. 10.1111/1755-0998.12538. PubMed DOI
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, et al.2010. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20:1297–1303. 10.1101/gr.107524.110. PubMed DOI PMC
Meier JI, Salazar PA, Kučka M, Davies RW, Dréau A, et al.2021. Haplotype tagging reveals parallel formation of hybrid races in two butterfly species. Proc Natl Acad Sci USA. 118:e2015005118. 10.1073/pnas.2015005118. PubMed DOI PMC
Meiklejohn CD, Landeen EL, Gordon KE, Rzatkiewicz T, Kingan SB, et al.2018. Gene flow mediates the role of sex chromosome meiotic drive during complex speciation. eLife. 7:e35468. 10.7554/eLife.35468. PubMed DOI PMC
Mitros T, Lyons JB, Session AM, Jenkins J, Shu S, et al.2019. A chromosome-scale genome assembly and dense genetic map for Xenopus tropicalis. Dev Biol. 452:8–20. 10.1016/j.ydbio.2019.03.015. PubMed DOI
Miura I. 2007. An evolutionary witness: the frog Rana rugosa underwent change of heterogametic sex from XY male to ZW female. Sex Dev. 1:323–331. 10.1159/000111764. PubMed DOI
Miura I. 2017. Sex determination and sex chromosomes in Amphibia. Sex Dev. 11:298–306. 10.1159/000485270. PubMed DOI
Morescalchi A. 1965. Osservazioni sulla cariologia di Bombina. Boll Zool. 32:207–219.
Morescalchi A, Galgano M.. 1973. Meiotic chromosomes and their taxonomic value in Amphibia Anura. Caldasia. 11:41–50.
Mudd AB. 2019. Comparative genomics and chromosome evolution [Ph.D. Thesis]. Berkeley: University of California. ProQuest ID: Mudd_berkeley_0028E_19261. Meritt ID: ark:/13030/m5vm9khh. https://escholarship.org/uc/item/1sp703wf.
Neves LG, Davis JM, Barbazuk WB, Kirst M.. 2013. Whole-exome targeted sequencing of the uncharacterized pine genome. Plant J. 75:146–156. 10.1111/tpj.12193. PubMed DOI
Nielsen R, Paul JS, Albrechtsen A, Song YS.. 2011. Genotype and SNP calling from next-generation sequencing data. Nat Rev Genet. 12:443–451. 10.1038/nrg2986. PubMed DOI PMC
Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A.. 2013. Assembling genomes and mini-metagenomes from highly chimeric reads. In: Deng M, Jiang R, Sun F, Zhang X, editors.. Research in Computational Molecular Biology, Lecture Notes in Computer Science. Berlin, Heidelberg: Springer. p. 158–170.
Nürnberger B, Lohse K, Fijarczyk A, Szymura JM, Blaxter ML.. 2016. Para-allopatry in hybridizing fire-bellied toads (Bombina bombina and B. variegata): inference from transcriptome-wide coalescence analyses. Evolution. 70:1803–1818. 10.1111/evo.12978. PubMed DOI PMC
Ogata M, Lambert M, Ezaz T, Miura I.. 2018. Reconstruction of female heterogamety from admixture of XX-XY and ZZ-ZW sex-chromosome systems within a frog species. Mol Ecol. 27:4078–4089. 10.1111/mec.14831. PubMed DOI
Olmo E, Morescalchi A, Stingo V, Odierna G.. 1982. Genome characteristics and the systematics of Discoglossidae (Amphibia, Salientia). Monitore Zool Ital (N.S.). 16:283–299.
Ouellette LA, Reid RW, Blanchard SG, Brouwer CR.. 2018. LinkageMapView—rendering high-resolution linkage and QTL maps. Bioinformatics. 34:306–307. 10.1093/bioinformatics/btx576. PubMed DOI PMC
Perrin N. 2009. Sex reversal: A fountain of youth for sex chromosomes? Evolution. 63:3043–3049. 10.1111/j.1558-5646.2009.00837.x. PubMed DOI
Piprek RP. 2013. Gonadogenesis in Anura: cellular and molecular mechanisms of sexual differentiation of gonads [PhD Thesis]. Kraków: Jagiellonian University.
Piprek RP, Pecio A, Szymura JM.. 2010. Differentiation and development of gonads in the Yellow-Bellied Toad, Bombina variegata L., 1758 (Amphibia: Anura: Bombinatoridae). Zool Sci. 27:47–55. PubMed
Poulter RTM, Goodwin TJD.. 2005. DIRS-1 and the other tyrosine recombinase retrotransposons. Cytogenet Genome Res. 110:575–588. 10.1159/000084991. PubMed DOI
Powell DL, García-Olazábal M, Keegan M, Reilly P, Du K, et al.2020. Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish. Science. 368:731–736. 10.1126/science.aba5216. PubMed DOI PMC
R Core Team. 2020. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
Rafińska A. 1991. Reproductive biology of the fire-bellied toads, Bombina bombina and B. variegata (Anura: Discoglossidae): egg size, clutch size and larval period length differences. Biol J Linn Soc. 43:197–210.
Ranallo-Benavidez TR, Jaron KS, Schatz MC.. 2020. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat Commun. 11:1432. 10.1038/s41467-020-14998-3. PubMed DOI PMC
Rastas P. 2017. Lep-MAP3: robust linkage mapping even for low-coverage whole genome sequencing data. Bioinformatics. 33:3726–3732. 10.1093/bioinformatics/btx494. PubMed DOI
Rieseberg LH, Baird SJE, Gardner KA.. 2000. Hybridization, introgression and linkage evolution. Plant Mol Biol. 42:205–224. PubMed
Rodrigues N, Betto-Colliard C, Jourdan-Pineau H, Perrin N.. 2013. Within-population polymorphism of sex-determination systems in the common frog (Rana temporaria). J Evol Biol. 26:1569–1577. 10.1111/jeb.12163. PubMed DOI
Rodrigues N, Vuille Y, Brelsford A, Merilä J, Perrin N.. 2016. The genetic contribution to sex determination and number of sex chromosomes vary among populations of common frogs (Rana temporaria). Heredity (Edinb). 117:25–32. 10.1038/hdy.2016.22. PubMed DOI PMC
Rodrigues N, Studer T, Dufresnes C, Perrin N.. 2018. Sex-chromosome recombination in Common Frogs brings water to the fountain-of-youth. Mol Biol Evol. 35:942–948. 10.1093/molbev/msy008. PubMed DOI
Rogers RL, Zhou L, Chu C, Márquez R, Corl A, et al.2018. Genomic takeover by transposable elements in the Strawberry Poison Frog. Mol Biol Evol. 35:2913–2927. doi:10.1093/molbev/msy185. PubMed PMC
Sachdeva H, Barton NH.. 2018. Introgression of a block of genome under infinitesimal selection. Genetics. 209:1279–1303. 10.1534/genetics.118.301018. PubMed DOI PMC
Sardell JM, Kirkpatrick M.. 2020. Sex differences in the recombination landscape. Am Nat. 195:361–379. 10.1086/704943. PubMed DOI PMC
Schumer M, Powell DL, Corbett‐Detig R.. 2020. Versatile simulations of admixture and accurate local ancestry inference with mixnmatch and ancestryinfer. Mol Ecol Resour. 20:1141–1151. 10.1111/1755-0998.13175. PubMed DOI PMC
Sedghifar A, Brandvain Y, Ralph P.. 2016. Beyond clines: lineages and haplotype blocks in hybrid zones. Mol Ecol. 25:2559–2576. 10.1111/mec.13677. PubMed DOI
Shchur V, Svedberg J, Medina P, Corbett-Detig R, Nielsen R.. 2020. On the distribution of tract lengths during adaptive introgression. G3 (Bethesda). 10:3663–3673. 10.1534/g3.120.401616. PubMed DOI PMC
Simpson JT, Durbin R.. 2012. Efficient de novo assembly of large genomes using compressed data structures. Genome Res. 22:549–556. 10.1101/gr.126953.111. PubMed DOI PMC
Simpson JT. 2014. Exploring genome characteristics and sequence quality without a reference. Bioinformatics. 30:1228–1235. 10.1093/bioinformatics/btu023. PubMed DOI PMC
Stöck M, Horn A, Grossen C, Lindtke D, Sermier R, et al.2011. Ever-young sex chromosomes in European tree frogs. PLoS Biol. 9:e1001062. PubMed PMC
Sun Y-B, Xiong Z-J, Xiang X-Y, Liu S-P, Zhou W-W, et al.2015. Whole-genome sequence of the Tibetan frog Nanorana parkeri and the comparative evolution of tetrapod genomes. Proc Natl Acad Sci USA. 112:E1257–E1262. 10.1073/pnas.1501764112. PubMed DOI PMC
Szymura JM. 1993. Analysis of hybrid zones with Bombina. In:Harrison RG, editor. Hybrid Zones and the Evolutionary Process. New York, NY: Oxford University Press. p. 261–289.
Szymura JM, Barton NH.. 1991. The genetic structure of the hybrid zone between the fire-bellied toads Bombina bombina and B. variegata: comparison between transects and between loci. Evolution. 45:237–261. PubMed
Szymura JM, Farana I.. 1978. Inheritance and linkage analysis of five enzyme loci in interspecific hybrids of toadlets, genus Bombina. Biochem Genet. 16:307–319. PubMed
Tamschick S, Rozenblut-Kościsty B, Bonato L, Dufresnes C, Lymberakis P, et al.2014. Sex chromosome conservation, DMRT1 phylogeny and gonad morphology in diploid Palearctic Green Toads (Bufo viridis Subgroup). Cytogenet Genome Res. 144:315–324. 10.1159/000380841. PubMed DOI
Toups MA, Rodrigues N, Perrin N, Kirkpatrick M.. 2019. A reciprocal translocation radically reshapes sex-linked inheritance in the common frog. Mol Ecol. 28:1877–1889. 10.1111/mec.14990. PubMed DOI PMC
Uecker H, Setter D, Hermisson J.. 2015. Adaptive gene introgression after secondary contact. J Math Biol. 70:1523–1580. 10.1007/s00285-014-0802-y. PubMed DOI PMC
Urry LA, Cain ML, Wasserman SA, Minorsky PV, Reece JB.. 2020. Campbell Biology. New York, NY: Pearson.
Vicoso B, Kaiser VB, Bachtrog D.. 2013. Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution. Proc Natl Acad Sci USA. 110:6453–6458. 10.1073/pnas.1217027110. PubMed DOI PMC
Volff J-N, Nanda I, Schmid M, Schartl M.. 2007. Governing sex determination in fish: regulatory putsches and ephemeral dictators. Sex Dev. 1:85–99. 10.1159/000100030. PubMed DOI
Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, et al.2007. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 8:973–982. 10.1038/nrg2165. PubMed DOI
Wolfram Research, Inc. 2019. Mathematica. Champaign, IL: Wolfram Research, Inc.
Yanchukov A, Hofman S, Szymura JM, Mezhzherin S, Morozov-Leonov SY, et al.2006. Hybridization of Bombina bombina and B. variegata (Anura, Discoglossidae) at a sharp ecotone in Western Ukraine: comparisons across transects and over time. Evolution. 60:583–600. 10.1111/j.0014-3820.2006.tb01139.x. PubMed DOI